Aurora kinase A suppresses metabolic stress-induced autophagic cell death by activating mTOR signaling in breast cancer cells

Oncotarget

Volumn 5, Issue 17, 2014, Pages 7498-7511

  Xu, Ling Zhi ^a,b   Long, Zi Jie ^c   Peng, Fei ^a,b   Liu, Yang ^a,b   Xu, Jie ^a,b   Wang, Chang ^a,b   Jiang, Lei ^a,b   Guo, Tao ^a,b   Kamran, Muhammad ^a,b   Li, Si Si ^a,b   Wang, Chun Li ^a,b   Wang, Hong Jiang ^a   Zhao, Yong Fu ^a   Wan, Xian Yao ^a   Liu, Quentin ^a,b,c  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

Aurora kinase; Autophagy; Breast cancer; Cell death; Metabolic stress

Indexed keywords

3 METHYLADENINE; AURORA A KINASE; AUTOPHAGY PROTEIN 5; GLYCOGEN SYNTHASE KINASE 3BETA; MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN; SMALL INTERFERING RNA; TOZASERTIB; AURKA PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; ATG5 GENE; AUTOPHAGY; BREAST CANCER CELL LINE; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; CORRELATIONAL STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME OVEREXPRESSION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; METABOLIC STRESS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; BREAST TUMOR; COMET ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL CULTURE; TUMOR CELL LINE; WESTERN BLOTTING;

APOPTOSIS; AURORA KINASE A; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; COMET ASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TOR SERINE-THREONINE KINASES; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 84907533088     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2241     Document Type: Article

References (51)

1. Baehrecke EH. Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol. 2005; 6(6):505-510.
2. Mizushima N. Autophagy: process and function. Genes & development. 2007; 21(22):2861-2873.
3. Levine B and Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008; 132(1):27-42.
4. Mizushima N, Levine B, Cuervo AM and Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2008; 451(7182):1069-1075.
5. Levine B and Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Developmental cell. 2004; 6(4):463-477.
6. Hsu PP and Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell. 2008; 134(5):703-707.
7. Mathew R and White E. Autophagy, stress, and cancer metabolism: what doesn't kill you makes you stronger. Cold Spring Harbor symposia on quantitative biology. 2011; 76:389-396.
8. Lozy F and Karantza V. Autophagy and cancer cell metabolism. Seminars in cell & developmental biology. 2012; 23(4):395-401.
9. Levine B and Yuan J. Autophagy in cell death: an innocent convict? J Clin Invest. 2005; 115(10):2679-2688.
10. Kroemer G and Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008; 9(12):1004-1010.
11. Chen Y, McMillan-Ward E, Kong J, Israels SJ and Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell death and differentiation. 2008; 15(1):171-182.
12. Rodriguez-Vargas JM, Ruiz-Magana MJ, Ruiz-Ruiz C, Majuelos-Melguizo J, Peralta-Leal A, Rodriguez MI, Munoz-Gamez JA, de Almodovar MR, Siles E, Rivas AL, Jaattela M and Oliver FJ. ROS-induced DNA damage and PARP-1 are required for optimal induction of starvation-induced autophagy. Cell research. 2012; 22(7):1181-1198.
13. Kanzawa T, Zhang L, Xiao L, Germano IM, Kondo Y and Kondo S. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene. 2005; 24(6):980-991.
14. Martin AP, Mitchell C, Rahmani M, Nephew KP, Grant S and Dent P. Inhibition of MCL-1 enhances lapatinib toxicity and overcomes lapatinib resistance via BAK-dependent autophagy. Cancer biology & therapy. 2009; 8(21):2084-2096.
15. Marumoto T, Zhang D and Saya H. Aurora-A-a guardian of poles. Nature reviews Cancer. 2005; 5(1):42-50.
16. Liu Q and Ruderman JV. Aurora A, mitotic entry, and spindle bipolarity. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(15):5811-5816.
17. Guan Z, Wang XR, Zhu XF, Huang XF, Xu J, Wang LH, Wan XB, Long ZJ, Liu JN, Feng GK, Huang W, Zeng YX, Chen FJ and Liu Q. Aurora-A, a negative prognostic marker, increases migration and decreases radiosensitivity in cancer cells. Cancer research. 2007; 67(21):10436-10444.
18. Huang XF, Luo SK, Xu J, Li J, Xu DR, Wang LH, Yan M, Wang XR, Wan XB, Zheng FM, Zeng YX and Liu Q. Aurora kinase inhibitory VX-680 increases Bax/Bcl-2 ratio and induces apoptosis in Aurora-A-high acute myeloid leukemia. Blood. 2008; 111(5):2854-2865.
19. Xu J, Wu X, Zhou WH, Liu AW, Wu JB, Deng JY, Yue CF, Yang SB, Wang J, Yuan ZY and Liu Q. Aurora-A identifies early recurrence and poor prognosis and promises a potential therapeutic target in triple negative breast cancer. PloS one. 2013; 8(2):e56919.
20. Lam AK, Ong K and Ho YH. Aurora kinase expression in colorectal adenocarcinoma: correlations with clinicopathological features, p16 expression, and telomerase activity. Hum Pathol. 2008; 39(4):599-604.
21. Wang LH, Xiang J, Yan M, Zhang Y, Zhao Y, Yue CF, Xu J, Zheng FM, Chen JN, Kang Z, Chen TS, Xing D and Liu Q. The mitotic kinase Aurora-A induces mammary cell migration and breast cancer metastasis by activating the Cofilin-F-actin pathway. Cancer Res. 2010; 70(22):9118-9128.
22. Wan XB, Fan XJ, Huang PY, Dong D, Zhang Y, Chen MY, Xiang J, Xu J, Liu L, Zhou WH, Lv YC, Wu XY, Hong MH and Liu Q. Aurora-A activation, correlated with hypoxia-inducible factor-1alpha, promotes radiochemoresistance and predicts poor outcome for nasopharyngeal carcinoma. Cancer Sci. 2012; 103(8):1586-1594.
23. Liu LL, Long ZJ, Wang LX, Zheng FM, Fang ZG, Yan M, Xu DF, Chen JJ, Wang SW, Lin DJ and Liu Q. Inhibition of mTOR pathway sensitizes acute myeloid leukemia cells to aurora inhibitors by suppression of glycolytic metabolism. Mol Cancer Res. 2013; 11(11):1326-1336.
24. Zou Z, Yuan Z, Zhang Q, Long Z, Chen J, Tang Z, Zhu Y, Chen S, Xu J, Yan M, Wang J and Liu Q. Aurora kinase A inhibition-induced autophagy triggers drug resistance in breast cancer cells. Autophagy. 2012; 8(12):1798-1810.
25. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012; 8(4):445-544.
26. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, Jin S and White E. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 2007; 21(13):1621-1635.
27. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, Degenhardt K, Chen G, Jin S and White E. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 2007; 21(11):1367-1381.
28. Dazert E and Hall MN. mTOR signaling in disease. Curr Opin Cell Biol. 2011; 23(6):744-755.
29. Laplante M and Sabatini DM. mTOR signaling in growth control and disease. Cell. 2012; 149(2):274-293.
30. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, Wang CY, He X, MacDougald OA, You M, Williams BO and Guan KL. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell. 2006; 126(5):955-968.
31. Zhai P, Sciarretta S, Galeotti J, Volpe M and Sadoshima J. Differential roles of GSK-3beta during myocardial ischemia and ischemia/reperfusion. Circulation research. 2011; 109(5):502-511.
32. Lin SY, Li TY, Liu Q, Zhang C, Li X, Chen Y, Zhang SM, Lian G, Liu Q, Ruan K, Wang Z, Zhang CS, Chien KY, Wu J, Li Q, Han J, et al. GSK3-TIP60-ULK1 signaling pathway links growth factor deprivation to autophagy. Science. 2012; 336(6080):477-481.
33. Long ZJ, Xu J, Yan M, Zhang JG, Guan Z, Xu DZ, Wang XR, Yao J, Zheng FM, Chu GL, Cao JX, Zeng YX and Liu Q. ZM 447439 inhibition of aurora kinase induces Hep2 cancer cell apoptosis in three-dimensional culture. Cell Cycle. 2008; 7(10):1473-1479.
34. Dar AA, Belkhiri A and El-Rifai W. The aurora kinase A regulates GSK-3beta in gastric cancer cells. Oncogene. 2009; 28(6):866-875.
35. Das G, Shravage BV and Baehrecke EH. Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb Perspect Biol. 2012; 4(6).
36. Karantza-Wadsworth V and White E. Role of autophagy in breast cancer. Autophagy. 2007; 3(6):610-613.
37. Azad MB, Chen Y, Henson ES, Cizeau J, McMillan-Ward E, Israels SJ and Gibson SB. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy. 2008; 4(2):195-204.
38. Wan XB, Long ZJ, Yan M, Xu J, Xia LP, Liu L, Zhao Y, Huang XF, Wang XR, Zhu XF, Hong MH and Liu Q. Inhibition of Aurora-A suppresses epithelial-mesenchymal transition and invasion by downregulating MAPK in nasopharyngeal carcinoma cells. Carcinogenesis. 2008; 29(10):1930-1937.
39. Gozuacik D and Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 2004; 23(16):2891-2906.
40. Debnath J, Muthuswamy SK and Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 2003; 30(3):256-268.
41. Chen N, Eritja N, Lock R and Debnath J. Autophagy restricts proliferation driven by oncogenic phosphatidylinositol 3-kinase in three-dimensional culture. Oncogene. 2013; 32(20):2543-2554.
42. Yang D, Liu H, Goga A, Kim S, Yuneva M and Bishop JM. Therapeutic potential of a synthetic lethal interaction between the MYC proto-oncogene and inhibition of aurora-B kinase. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(31):13836-13841.
43. Schmukler E, Grinboim E, Schokoroy S, Amir A, Wolfson E, Kloog Y and Pinkas-Kramarski R. Ras inhibition enhances autophagy, which partially protects cells from death. Oncotarget. 2013; 4(1):142-152.
44. Kondo Y, Kanzawa T, Sawaya R and Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer. 2005; 5(9):726-734.
45. Ng S, Wu YT, Chen B, Zhou J and Shen HM. Impaired autophagy due to constitutive mTOR activation sensitizes TSC2-null cells to cell death under stress. Autophagy. 2011; 7(10):1173-1186.
46. Yuan HX, Russell RC and Guan KL. Regulation of PIK3C3/VPS34 complexes by MTOR in nutrient stress-induced autophagy. Autophagy. 2013; 9(12):1983-1995.
47. Vinayak S and Carlson RW. mTOR inhibitors in the treatment of breast cancer. Oncology. 2013; 27(1):38-44, 46, 48 passim.
48. Panieri E, Toietta G, Mele M, Labate V, Ranieri SC, Fusco S, Tesori V, Antonini A, Maulucci G, De Spirito M, Galeotti T and Pani G. Nutrient withdrawal rescues growth factor-deprived cells from mTOR-dependent damage. Aging (Albany NY). 2010; 2(8):487-503.
49. Yecies JL and Manning BD. mTOR links oncogenic signaling to tumor cell metabolism. J Mol Med (Berl). 2011; 89(3):221-228.
50. Vucicevic L, Misirkic M, Janjetovic K, Vilimanovich U, Sudar E, Isenovic E, Prica M, Harhaji-Trajkovic L, Kravic-Stevovic T, Bumbasirevic V and Trajkovic V. Compound C induces protective autophagy in cancer cells through AMPK inhibition-independent blockade of Akt/mTOR pathway. Autophagy. 2011; 7(1):40-50.
51. Speit G and Rothfuss A. The comet assay: a sensitive genotoxicity test for the detection of DNA damage and repair. Methods in molecular biology. 2012; 920:79-90.